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The niche conservatism hypothesis states that related species diverge in niche characteristics at lower rates than expected, given their lineage divergence. Here we analyze whether niche conservatism is a common pattern among vector species (Hemiptera: Reduviidae: Triatominae) of Trypanosoma cruzi that inhabit North and Central America, a highly heterogeneous landmass in terms of environmental gradients. Mitochondrial and nuclear loci were used in a multi-locus phylogenetic framework to reconstruct phylogenetic relationships among species and estimate time of divergence of selected clades to draw biogeographic inferences. Then, we estimated similarity between the ecological niche of sister species and tested the niche conservatism hypothesis using our best estimate of phylogeny. Triatoma is not monophyletic. A primary clade with all North and Central American (NCA) triatomine species from the genera Triatoma, Dipetalogaster, and Panstrongylus, was consistently recovered. Nearctic species within the NCA clade (T. p. protracta, T. r. rubida) diverged during the Pliocene, whereas the Neotropical species (T. phyllosoma, T. longipennis, T. dimidiata complex) are estimated to have diverged more recently, during the Pleistocene. The hypothesis of niche conservatism could not be rejected for any of six sister species pairs. Niche similarity between sister species best fits a retention model. While this framework is used here to infer niche evolution, it has a direct impact on spatial vector dynamics driven by human population movements, expansion of transportation networks and climate change scenarios., Author Summary Knowledge regarding the evolutionary history of insect vectors of pathogens is essential to design precise and appropriately integrated control strategies, since species' dispersal and invasive capacity are key components to prevent human-vector interaction. Given several well-known invasive or dispersal events of Triatominae, and their adaptive capacity to colonize modified habitats, the question arises whether niche conservatism (i.e. the limited capacity for niche differentiation within clades) across sister species could influence distribution patterns. Niche conservatism is herein analyzed across the highly heterogeneous landmass of North and Central America where most species complexes of the Triatominae are vectors of Trypanosoma cruzi. Since phylogenetic relationships among and within triatomine species complexes are still ill-defined, we first used a multi-locus phylogenetic analysis using mitochondrial and nuclear loci to validate relationships between species. Similarity of the ecological niche between six sister species' pairs was used to test the niche conservatism hypothesis. The results provide robust evidence of monophyly for North and Central America triatomine species. The hypothesis of niche conservatism was not rejected for any sister species pair, independently of niche width, distribution range, biogeographic affinity, or environmental heterogeneity; niche similarity correlated inversely with taxa divergence and according to a retention model.

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1 Insect Pest Control Laboratory, Joint Food and Agriculture Organization/International Atomic Energy Agency (FAO/IAEA) Programme of Nuclear Techniques in Food and Agriculture, Vienna, Austria, 2 Centre de cooperation internationale en recherche agronomique pour le developpement (CIRAD), Unite Mixte de Recherche Controle des Maladies Animales Exotiques et Emergentes, Montpellier, France, 3 Institut National de Recherche Agricole, Unite Mixte de Recherche 1309 Controle des Maladies Animales Exotiques et Emergentes, Montpellier, France, 4 Ministry of Agriculture, Natural Resources and Environment, Zanzibar, Tanzania, 5 Direction Nationale de l’Appui au Monde Rural, Unite Centrale de Lutte contre les Mouches Tse-Tse et les Trypanosomoses Animales, Bamako, Mali, 6 Pan-African Tsetse and Trypanosomosis Eradication Campaign (PATTEC), Projet de Creation de Zones Liberees Durablement de Tse-tse et de Trypanosomoses (PCZLD), Bobo-Dioulasso, Burkina Faso, 7 Food and Agriculture Organization of the United Nations (FAO), Animal Production and Health Division, Viale delle Terme di Caracalla, Rome, Italy, 8 Institut Senegalais de Recherches Agricoles, Laboratoire National d’Elevage et de Recherches Veterinaires, Dakar–Hann, Senegal

The authors have declared that no competing interests exist. The study was supported through a grant from the Department for International Development (DFID) and GlaxoSmithKline (GSK) for research on the elimination of lymphatic filariasis. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Background Establishing the sources of reinfestation after residual insecticide spraying is crucial for vector elimination programs. Triatoma infestans, traditionally considered to be limited to domestic or peridomestic (abbreviated as D/PD) habitats throughout most of its range, is the target of an elimination program that has achieved limited success in the Gran Chaco region in South America. Methodology/Principal Findings During a two-year period we conducted semi-annual searches for triatomine bugs in every D/PD site and surrounding sylvatic habitats after full-coverage spraying of pyrethroid insecticides of all houses in a well-defined rural area in northwestern Argentina. We found six low-density sylvatic foci with 24 T. infestans in fallen or standing trees located 110–2,300 m from the nearest house or infested D/PD site detected after insecticide spraying, when house infestations were rare. Analysis of two mitochondrial gene fragments of 20 sylvatic specimens confirmed their species identity as T. infestans and showed that their composite haplotypes were the same as or closely related to D/PD haplotypes. Population studies with 10 polymorphic microsatellite loci and wing geometric morphometry consistently indicated the occurrence of unrestricted gene flow between local D/PD and sylvatic populations. Mitochondrial DNA and microsatellite sibship analyses in the most abundant sylvatic colony revealed descendents from five different females. Spatial analysis showed a significant association between two sylvatic foci and the nearest D/PD bug population found before insecticide spraying. Conclusions Our study shows that, despite of its high degree of domesticity, T. infestans has sylvatic colonies with normal chromatic characters (not melanic morphs) highly connected to D/PD conspecifics in the Argentinean Chaco. Sylvatic habitats may provide a transient or permanent refuge after control interventions, and function as sources for D/PD reinfestation. The occurrence of sylvatic foci of T. infestans in the Gran Chaco may pose additional threats to ongoing vector elimination efforts., Author Summary Triatoma infestans, a highly domesticated species and historically the main vector of Trypanosoma cruzi, is the target of an insecticide-based elimination program in the southern cone countries of South America since 1991. Only limited success has been achieved in the Gran Chaco region due to repeated reinfestations. We conducted full-coverage spraying of pyrethroid insecticides of all houses in a well-defined rural area in northwestern Argentina, followed by intense monitoring of house reinfestation and searches for triatomine bugs in sylvatic habitats during the next two years, to establish the putative sources of new bug colonies. We found low-density sylvatic foci of T. infestans in trees located within the species' flight range from the nearest infested house detected before control interventions. Using multiple methods (fine-resolution satellite imagery, geographic information systems, spatial statistics, genetic markers and wing geometric morphometry), we corroborated the species identity of the sylvatic bugs as T. infestans and found they were indistinguishable from or closely related to local domestic or peridomestic bug populations. Two sylvatic foci were spatially associated to the nearest peridomestic bug populations found before interventions. Sylvatic habitats harbor hidden foci of T. infestans that may represent a threat to vector suppression attempts.